Co-inoculation of rhizobia, azospirilla and cyanobacteria for increasing common bean production

Eduardo Hélder Horácio, Claudemir Zucareli, Freddy Zambrano Gavilanes, João Sarkis Yunes, Alisson Wilson dos Santos Sanzovo, Diva Souza Andrade

Abstract


The combined inoculation of Rhizobium (R. tropici+R. freirei), Azospirillum brasilense, and Anabaena cylindrica, a diazotrophic cyanobacterium, is a technology that has not yet been tested and established in the production of the common bean (Phaseolus vulgaris). The inoculation may be a promising strategy for increasing crop productivity by combining the benefits of biological nitrogen fixation with the production of plant growth phytohormones. Therefore, the objective of this study was to evaluate the co-inoculation of Rhizobium, Azospirillum brasilense, and Anabaena cylindrica as an alternative method for optimizing the symbiotic performance and development of the common bean at greenhouse conditions. The treatments were as follows: (T1) control without N and inoculation, (T2) N addition (100 kg N ha-1), (T3) Riz (addition of R. tropici+R. freirei), (T4) Azo (Azospirillum brasilense addition), (T5) Ana (Anabaena cylindrical addition), (T6) Riz+Azo, (T7) Riz+Ana, (T8) Azo+Ana, (T9) Riz+Azo+Ana. We used a completely randomized experimental design with four replications. The co-inoculation of Riz+Azo+Ana promoted plant height, root length and volume, shoot dry matter, accumulated shoot N, number and dry matter of nodules at flowering, number of grains per pod, hundred seed weight, and grain production of the common bean, contributing to increased yield per plant. We observed an increase in common bean grain yield ranging from 62 to 84% after double and triple co-inoculation of rhizobia with azospirilla and/or cyanobacteria, with the highest yield observed in the plants inoculated with Riz+Azo+Ana (84%), similar to those observed in plants after N addition. However, field experiments are necessary to elucidate the performances of the inoculated beneficial microorganisms.

Keywords


Anabaena cylindrica; Azospirillum brasilense; Phaseolus vulgaris; Rhizobium freirei; Rhizobium tropici.

Full Text:

PDF

References


Andrade, D. S., Machineski, G. S., Lovato, G. M., Colozzi, A., Fº., & Goes, K. C. G. P. de. (2014). Inoculação de microalgas em leguminosas e gramíneas. In D. S., Andrade., & A. Colozzi, Fº. (Eds.), Microalgas de águas continentais: desafios e potencialidades do cultivo (Vol 2, pp. 413-438), Londrina: IAPAR.

Bashan, Y., Bashan, L. de, Prabhu, S. R., & Hernandez, J.-P. (2014). Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998-2013). Plant and Soil, 378(1), 1-33. doi: 10.1007/s11104-013-1956-x

Bremner, J., & Keeney, D. (1965). Steam distillation methods for determination of ammonium, nitrate and nitrite. Analytica Chimica Acta, 32(1), 482-485. doi: 10.1016/S0003-2670(00)88973-4.

Cardoso, J. D., Hungria, M., & Andrade, D. S. (2012). Polyphasic approach for the characterization of rhizobial symbionts effective in fixing N2 with common bean (Phaseolus vulgaris L.) Applied Microbiology and Biotechnology, 93(5), 2035-2049. doi: 10.1007/s00253-011-3708-2

Dall'Agnol, R. F., Ribeiro, R. A., Ormeno-Orrillo, E., Rogel, M. A., Delamuta, J. R. M., Andrade, D. S., Martínez-Romero, E., Hungria, M. (2013). Rhizobium freirei sp. nov., a symbiont of Phaseolus vulgaris that is very effective at fixing nitrogen. nternational Journal of Systematic and Evolutionary Microbiology, 63(11), 4167-4173. doi: 10.1099/ijs.0.052928-0

Egamberdieva, D., Berg, G., Lindström, K., & Räsänen, L. A. (2010). Co-inoculation of Pseudomonas spp. with Rhizobium improves growth and symbiotic performance of fodder galega (Galega orientalis Lam.). European Journal of Soil Biology, 46(3), 269-272. doi: 10.1016/j.ejsobi.2010.01.005

Ferreira, D. F. (2011). Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia, 35(6), 1039-1042. doi: 10.1590/S1413-70542011000600001

Fukami, J., Cerezini, P., & Hungria, M. (2018). Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Express, 8(73), 1-12. doi: 10.1186/s13568-018-0608-1

Fukami, J., Nogueira, M. A, Araujo, R. S., & Hungria, M. (2016). Accessing inoculation methods of maize and wheat with Azospirillum brasilense. AMB Express, 6(3), 1-13. doi: 10.1186/s13568-015-0171-y

Gange, A. C., & Gadhave, K. R. (2018). Plant growth-promoting rhizobacteria promote plant size inequality. Scientific Reports, 8(1), 13828. doi: 10.1038/s41598-018-32111-z

Ghaderiardakani, F., Collas, E., Damiano, D. K., Tagg, K., & Graham, N. S. (2019). Effects of green seaweed extract on Arabidopsis early development suggest roles for hormone signalling in plant responses to algal fertilisers. Scientific Reports, 9(1), 1-13. doi: 10.1038/s41598-018-38093-2

Gordillo-Delgado, F., Marín, E., & Calderón, A. (2016). Effect of Azospirillum brasilense and Burkholderia unamae bacteria on maize photosynthetic activity evaluated using the photoacoustic technique. International Journal of Thermophysics, 37(9), 1-11. doi: 10.1007/s10765-016-2101-x

Hungria, M., Andrade, D. S., Chueire, L. M. D. O., Probanza, A., Guttierrez-Manero, F. J., Megias, M. (2000). Isolation and characterization of new efficient and competitive bean (Phaseolus vulgaris L.) rhizobia from Brazil. Soil Biology & Biochemistry, 32(11-12), 1515-1528. doi: 10.1016/S0038-0717 (00)00063-8

Hungria, M., Nogueira, M. A., & Araujo, R. S. (2013). Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability. Biology and Fertility of Soils, 49(7), 791-801. doi: 10.1007/s00374-012-0771-5

Jaiswal, P., Prasanna, R., Nayak, S., Sood, A., & Suseela, M. (2008). Characterization of rhizo-cyanobacteria and their associations with wheat seedlings. Egyptian Journal of Biology, 10(1), 20-27.

Kazi, N., Deaker, R., Wilson, N., Muhammad, K., & Trethowan, R. (2016). The response of wheat genotypes to inoculation with Azospirillum brasilense in the field. Field Crops Research, 196(1), 368-378. doi: 10.1016/j.fcr.2016.07.012

Korir, H., Mungai, N. W., Thuita, M., Hamba, Y., & Masso, C. (2017). Co-inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in a low phosphorus soil. Frontiers in Plant Science, 8(141), 1-10. doi: 10.3389/fpls.2017.00141

Loreto, C., Rosales, N., Bermúdez, J., & Morales, E. (2003). Produccion de pigmentos y proteinas de la cianobacteria Anabaena pcc 7120 en relacion a la concentracion de nitrogeno e irradiancia. Gayana Botánica, 60(6), 83-89. doi: 10.4067/S0717-66432003000200001.

Manjunatha, M., Kanchan, A., Ranjan, K., Venkatachalam, S., Prasanna, R., Ramakrishnan, B., Singh, B. (2016). Beneficial cyanobacteria and eubacteria synergistically enhance bioavailability of soil nutrients and yield of okra. Heliyon, 2(2), 1-28. doi: 10.1016/j.heliyon.2016.e00066

Mulas, D., Seco, V., Casquero, P. A., Velázquez, E., & González-Andrés, F. (2015). Inoculation with indigenous rhizobium strains increases yields of common bean (Phaseolus vulgaris L.) in northern Spain, although its efficiency is affected by the tillage system. Symbiosis, 67(3), 113-124. doi: 10.1007/ s13199-015-0359-6

Parra, M. S., & Oliveira, E. L. (2003). Sugestão de adubação e calagem para culturas de interesse econômico no Estado do Paraná. In: Oliveira, E. L., Feijão (128a ed., pp. 17-18). (Circular Técnica). Londrina: IAPAR.

Peres, A. R., Rodrigues, R. A. F., Arf, O., Portugal, J. R., & Corsini, D. C. D. C. (2016). Co-inoculation of Rhizobium tropici and Azospirillum brasilense in common beans grown under two irrigation depths. Revista Ceres, 63(2), 198-207. doi: 10.1590/0034-737X201663020011

Piotrowska-Niczyporuk, A., Bajguz, A., Kotowska, U., Bralska, M., & Talarek-Karwel, M. (2018). Growth, metabolite profile, oxidative status, and phytohormone levels in the green alga Acutodesmus obliquus exposed to exogenous auxins and cytokinins. Journal of Plant Growth Regulation, 37(4), 1159-1174. doi: 10.1007/s00344-018-9816-9

Rencher, A. (2002). Methods of multivariate analysis (2nd ed.). New York: A John Wiley & Sons, Inc. Publication.

Renuka, N., Guldhe, A., Prasanna, R., Singh, P., & Bux, F. (2018). Microalgae as multi-functional options in modern agriculture: current trends, prospects and challenges. Biotechnology advances, 36(4), 1255-1273. doi: 10.1016/j.biotechadv.2018.04.004

Rodrigues, A., Antunes, J., Medeiros, V. D. E., Barros, B. D. F., & Figueiredo, M. D. V. (2012). Co-inoculation response of growth promoting bacterias in plants and Bradyrhizobium sp. in cowpea. Bioscience Journal, 28(1), 196-202.

Schossler, J., Meert, L., Rizzardi, D., & Michalovicz, L. (2016). Yield components and grain yield of common-bean submitted to the inoculation and co-inoculation of Rhizobium tropici and Azospirillum brasilense strains. Revista Scientia Agraria, 17(1), 10-15. doi: 10.5380/rsa.v17i1

Soares, B. L., Ferreira, P. A. A., Rufini, M., Martins, F. A. D., Oliveira, D. P., Reis, R. P., Moreira, F. M. de S. (2016). Agronomic and economic efficiency of common-bean inoculation with rhizobia and mineral nitrogen fertilization. Revista Brasileira de Ciência do Solo, 40(1), 10-15. e0150235. doi: 10.1590/ 18069657rbcs20150235

Soil Survey Staff (2014). Keys to oil taxonomy (12nd ed.). Washington, DC: Natural Resources Conservation Service. Natural Resources Conservation Service (NRCS), United States Department of Agriculture (USDA).

Stajkovi?, O., Deli?, D., Joši?, D., Kuzmanovi?, ?., Rasuli?, N., & Kneževi?-Vuk?evi?, J. (2011). Improvement of common bean growth by co-inoculation with Rhizobium and plant growth-promoting bacteria. Romanian Biotechnological Letters, 16(1), 5919-5926.

Steiner, F., Ferreira, H. C. P., & Zuffo, A. M., (2019). Can co-inoculation of Rhizobium tropici and Azospirillum brasilense increase common bean nodulation and grain yield? Semina: Ciências Agrárias, 40(1), 81-98. doi: 10.5433/1679-0359.

Tate, J. J., Gutierrez-Wing, M. T., Rusch, K. A., & Benton, M. G. (2013). The effects of plant growth substances and mixed cultures on growth and metabolite production of green algae Chlorella sp.: a review Journal of Plant Growth Regulation, 32(2), 417-428. doi: 10.1007/s00344-012-9302-8

Wirtz, N. L., Treble, R. G., & Weger, H. G. (2010). Siderophore-independent iron uptake by iron-limited cells of the cyanobacterium Anabaena flos-aquae. Journal of Phycology, 46(5), 947-957. doi: 10.1111/ j.1529-8817.2010.00881.x

Yadegari, M. (2014). Evaluation of bean (Phaseolus vulgaris) seeds’ inoculation with Rhizobium phaseoli and plant growth promoting rhizobacteria (PGPR) on yield and yield components. Advances in Environmental Biology, 8(2), 419-424.

Yagi, R., Andrade, D. S., Waureck, A., & Gomes, J. C. (2015). Nodulations and grain yields of common beans in response to nitrogen fertilization or seed inoculation with Rhizobium freirei. Revista Brasileira de Ciência do Solo, 39(6), 1661-1670. doi: 10.1590/0100068rbcs20140342




DOI: http://dx.doi.org/10.5433/1679-0359.2020v41n5supl1p2015

Semina: Ciênc. Agrár.
Londrina - PR
E-ISSN 1679-0359
DOI: 10.5433/1679-0359
E-mail: semina.agrarias@uel.br
Este obra está licenciado com uma Licença Creative Commons Atribuição-NãoComercial 4.0 Internacional